REVIEW published: 03 July 2018 doi: 10.3389/fevo.2018.00093

Multimodal Aposematic Signals and Their Emerging Role in Mate Attraction

Bibiana Rojas 1*, Emily Burdfield-Steel 1, Chiara De Pasqual 1†, Swanne Gordon 1†, Linda Hernández 1†, Johanna Mappes 1†, Ossi Nokelainen 1†, Katja Rönkä 1,2† and Carita Lindstedt 1

1 Department of Biological and Environmental Science, Centre of Excellence in Biological Interactions, University of Jyvaskyla, Jyväskylä, Finland, 2 Faculty of Biological and Environmental Sciences, Organismal and Evolutionary Biology Research Programme, University of Helsinki, Helsinki, Finland

Chemically defended animals often display conspicuous color patterns that predators Edited by: learn to associate with their unprofitability and subsequently avoid. Such animals (i.e., Varvara Yu. Vedenina, Institute for Information Transmission aposematic), deter predators by stimulating their visual and chemical sensory channels. Problems (RAS), Russia Hence, aposematism is considered to be “multimodal.” The evolution of warning signals Reviewed by: (and to a lesser degree their accompanying chemical defenses) is fundamentally linked Ximena J. Nelson, to natural selection by predators. Lately, however, increasing evidence also points to a University of Canterbury, New Zealand Fabio Cortesi, role of sexual selection shaping warning signal evolution. One of the species in which this The University of Queensland, has been shown is the wood tiger moth, Arctia plantaginis, which we here put forward Australia as a promising model to investigate multimodality in aposematic and sexual signaling. *Correspondence: Bibiana Rojas A. plantaginis is an aposematic diurnal moth which exhibits sexually dimorphic coloration bibiana.rojas@jyu.fi as well as sex-limited polymorphism in part of its range. The anti-predator function

†Authors’ names in alphabetical order. of its coloration and, more recently, its chemical defenses (even when experimentally decoupled from the visual signals), has been well-demonstrated. Interestingly, recent Specialty section: studies have revealed differences between the two male morphs in mating success, This article was submitted to Behavioral and Evolutionary Ecology, suggesting a role of coloration in mate choice or attraction, and providing a possible a section of the journal explanation for its sexual dimorphism in coloration. Here, we: (1) review the lines of Frontiers in Ecology and Evolution evidence showing the role of predation pressure and sexual selection in the evolution Received: 01 May 2018 of multimodal aposematic signals in general, and in the wood tiger moth in particular; Accepted: 13 June 2018 Published: 03 July 2018 (2) establish gaps in current research linking sexual selection and predation as selective Citation: pressures on aposematic signals by reviewing a sample of the literature published in Rojas B, Burdfield-Steel E, De the last 30 years; (3) highlight the need of identifying suitable systems to address Pasqual C, Gordon S, Hernández L, simultaneously the effect of natural and sexual selection on multimodal aposematic Mappes J, Nokelainen O, Rönkä K and Lindstedt C (2018) Multimodal signals; and (4) propose directions for future research to test how aposematic signals Aposematic Signals and Their can evolve under natural and sexual selection. Emerging Role in Mate Attraction. Front. Ecol. Evol. 6:93. Keywords: warning coloration, multimodal signals, predator-prey interactions, sexual selection, chemical signals, doi: 10.3389/fevo.2018.00093 signal variation

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INTRODUCTION dorsal markings signal potential mates (Robertson and Monteiro, 2005). Animals can communicate their quality to potential mates or One way to increase the efficacy of a particular signal predators with different types of signals (Maynard Smith and is to stimulate multiple sensory modalities of the receiver Harper, 2003). Because signals may be targeted to different simultaneously (Partan and Marler, 1999). This type of receivers, the multiple functions can sometimes lead to a conflict multimodal signals are used in the aposematic displays that between natural and sexual selection, which imposes limitations defended organisms use to advertise their unprofitability (e.g., on signal evolution. For instance, in Darwin and Fisher’s sexual toxicity, unpalatability, or physical defenses such as spines) to selection theories (Darwin, 1869; Fisher, 1930), some traits can potential predators (Poulton, 1890; Cott, 1940; Edmunds, 1974; be favored by sexual selection, such as the vivid body colors Ruxton et al., 2004; Rojas et al., 2015b). Multimodal signals on a male guppy, Poecilia reticulata (Endler, 1988b; Figure 1A), are also common in sexual communication where males can but the evolution of these conspicuous ornaments may be advertise their quality via multiple cues in multiple sensory constrained by the individual’s survival, as they are also easier channels (Bradbury and Vehrencamp, 2011). More recently, it to detect by predators or parasites (Endler, 1988b; Kotiaho et al., has become evident that certain visual components, such as 1998; Zuk and Kolluru, 1998; Lindström et al., 2005). Likewise, bright color patterns, in multimodal displays may have a dual females of the Túngara frog, Engystomops pustulosus, prefer male function both as aposematic and sexual signals (Cummings mating calls of increased complexity which, in turn, are easier and Crothers, 2013). In contrast, much less information exists to detect and locate by bats (Ryan et al., 1982; Figure 1C); and on whether or not secondary defenses could also have a dual females of the wolf spider Hygrolycosa rubrofasciata (Figure 1D) function in both chemical communication to potential predators prefer males that drum their abdomen against the dry leaves and potential mates (Conner et al., 1981). at higher rates (Parri et al., 1997), which can lead to increased Here, we: (1) review the multiple lines of evidence showing predation risk (Kotiaho et al., 1998). However, if different both how predation pressure has shaped the evolution of elements of the signal are targeted to a different receiver or evoke multimodal aposematic signals, as well as the less studied role different responses, then they can evolve despite being the subject of sexual selection in warning color evolution; (2) establish the of both selective factors (Endler, 1992; Figure 1). That is the case gaps in current studies linking sexual selection and predation in the dorsal and ventral markings in the wings of butterflies as selective pressures on the warning displays of aposematic of the genus Bicyclus (Oliver et al., 2009), such as B. Anynana species, by reviewing a sample of the literature published over (Figure 1B). While the eyespots on the ventral side of their wings the last 30 years; (3) point out the need to identify representative deter predators (Lyytinen et al., 2004), the UV reflection of the model systems from different taxonomic groups where both

FIGURE 1 | Examples of organisms whose signals are under the influence of both sexual and natural selection. (A) Trinidadian guppy, Poecilia reticulata. Females prefer signals that are also an easier target for predators; (B) Squinting Bush-brown, Bicyclus anynana. The eyespot markings on the ventral side of their wings deter predators, while dorsal markings signal to potential mates; (C) Túngara frog, Engystomops pustulosus. Females prefer signals of higher complexity, which are also easier to detect by predators such as bats; and (D) Wolf spider Hygrolycosa rubrofasciata. Males vibrate their abdomen against the dry leaf substrate producing a drumming that is even audible for humans. Females prefer males with a high drumming rate, yet a high drumming rate can lead to increased predation risk. Photos: (A) PH Olsen CC BY 3.0, Wikimedia Commons; (B) Oskar Brattström; (C) R. Taylor; (D) Sanja565658 CC BY-SA 3.0, Wikimedia Commons.

Frontiers in Ecology and Evolution | www.frontiersin.org 2 July 2018 | Volume 6 | Article 93 Rojas et al. Aposematic Signals and Mate Attraction the function and ecological significance of coloration and Multimodal signals are thought to improve associative compounds used in chemical communication are well-known, to learning because they provide more information per unit of time understand the interplay between sexual selection and selection than uni-modal displays (Partan and Marler, 2005) and, thus, the by predators on the different components of multimodal signals. interaction between multiple types of signals is often expected to To this end, we use the wood tiger moth A. plantaginis as a be more efficient than each signal on its own. However, there are case study; and (4) suggest specific paths for future research various types of multimodal signals, which differ in the type of to test how aposematic signals can be used in mating contexts, response they elicit in the receiver, depending on whether each and evolve under (the interacting effects of) natural and sexual component acts independently, exerts dominance or modulation selection. over the other signal(s), or give rise to an entirely new response (Partan and Marler, 1999). With the coupling of a warning signal and a secondary APOSEMATISM IS INHERENTLY (e.g., chemical) defense, aposematic organisms are capable of deterring predators by stimulating, for example, their visual MULTIMODAL and olfactory/gustatory (chemical) sensory channels. Therefore, aposematism is inherently multimodal (Rowe and Guilford, Animal displays often consist of several components (Bradbury 1999; Rowe and Halpin, 2013). The most common primary and Vehrencamp, 2011). When multiple components stimulate defense in warning displays is warning coloration (visual different sensory systems in the receiver, for example the visual component). To ensure its efficacy as a signal, warning and the auditory (Figure 2A), these displays are considered coloration is expected to be conspicuous and distinctive, and multimodal (Partan and Marler, 1999; Higham and Hebets, therefore easy to learn and memorize, as all these characteristics 2013). If these multiple components, however, elicit receiver facilitate predator’s associative learning (Cott, 1940). In fact, responses in the same sensory modality, these displays are predators seem to remember the association between aposematic not considered multimodal and are referred to simply as signals and unprofitability for longer than when learned for multicomponent (Partan and Marler, 2005; Bradbury and unprofitable cryptic species (Roper and Redston, 1987; Roper, Vehrencamp, 2011; Higham and Hebets, 2013). For example, 1994). Red, orange, and yellow have been suggested to be a visual signal may contain several components such as color, efficient warning signals given their color constancy under varied pattern, and size (Figure 2B), which may even provide different light environments, and their high contrast against different information to the receiver, but in the end only stimulates one backgrounds (Stevens and Ruxton, 2012; Figure 3). Likewise, sensory (visual) modality (Rowe, 1999). color patterns with high internal contrast, such as black and white or black and yellow, have been proven to be learned faster (Zylinski and Osorio, 2013). In addition to visual signals, sounds such as the buzz of bumblebees (Siddall and Marples, 2011) or the ultrasonic clicks of some tiger moth species (Dunning and Kruger, 1995; Hristov and Conner, 2005; Ratcliffe and Nydam, 2008) have shown to protect defended prey from predators such as birds and bats, respectively. Likewise, skunks use warning sounds and behaviors to advertise the possession of chemical defenses, which they only spray if absolutely necessary (Andersen et al., 1982; Lartviere and Messier, 1996). Interestingly, although not conducted with the purpose of studying warning displays, a study by Tuttle and Ryan (1981) showed that the frog-eating bat, Trachops cirrhosus, is capable of distinguishing edible from unpalatable frogs on the basis of their mating calls (Tuttle and Ryan, 1981), hinting at a prominent role of warning signals of different sensory modalities in the deterrence of non-visually-oriented predators.

FIGURE 2 | Illustration of the difference between (A) multimodal and (B) Among secondary defenses, the most prominent are defensive multicomponent signals. (A) The strawberry poison frog, Oophaga pumilio, chemicals. Examples of chemical defenses in vertebrates include has both visual (color) and acoustic (call) signals. While both are involved in the alkaloids found in poison frogs (Saporito et al., 2012; Santos sexual selection (Maan and Cummings, 2012; Dreher and Pröhl, 2014), these et al., 2016), the tetrodotoxins found in some newts, pufferfish stimulate different sensory (visual and auditory) channels or modes in the and some harlequin toads (Mosher et al., 1964; Kim et al., 1975), receiver. (B) The butterfly Heliconius erato has both color and pattern components to its visual signal (Finkbeiner et al., 2014). These may (or may and the disulfides (among other compounds) sprayed by skunks not) encode different information, but stimulate the same sensory channel or (Andersen et al., 1982). Among invertebrates, some common mode (vision) in the receiver. Note that we are here focusing only on the visual defensive compounds are the iridoid glycosides (Lindstedt et al., signal of this butterfly for the purpose of illustrating multicomponency. H. erato 2010; Reudler et al., 2015), cardenolides, pyrrolizidine alkaloids, is also chemically defended and the combination of its secondary defences pyrazines, and cyanide compounds found in numerous insects and its visual signal make up their multimodal aposematic display. (Rothschild et al., 1979, 1984; Bowers, 1992), as well as the

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FIGURE 3 | Aposematism is widespread across the animal kingdom. (A) Harlequin bug, Tectocoris diophthalmus; (B) Eastern newt (eft form), Notophtalmus viridescens; (C) Burnet moths, Family Zygaenidae; (D) Sea slug, Chomodoris annae; (E) Eastern coral snake, Micrurus fluvius; (F) Appalachian mountains millipede, Apheloria polychroma; (G) Harlequin poison frog, Oophaga occultator; (H) ladybird, family Coccinelidae. Photos: (A) E. Burdfield-Steel; (B,D) JP Lawrence; (C,H) B. Rojas; (E) N. Scobel; (F) P. Marek; (G) P. Palacios. furanosesquiterpenes and diterpenes (among others) found in communication (Figure 4). That is, for example, markings nudibranch molluscs (Winters et al., 2018). These defenses may allowing individual recognition (Figure 4B), or sexually selected stimulate the olfactory or gustatory channels, or both. traits being modified to have a double function (to ward- off would-be predators and either indicate status, or attract potential mates) once the species had developed an effective THE INTERPLAY BETWEEN NATURAL AND secondary defense (Mallet and Singer, 1987). Given our focus on SEXUAL SELECTION IN SHAPING aposematism we will primarily discuss natural selection imposed MULTIMODAL APOSEMATIC SIGNALS by predation pressure for the remainder of this review. The evolution of warning signals via natural selection may Although there is no consensus about how aposematic coloration be coupled with sexual selection in both a stabilizing or initially evolved, it has been suggested that it may have diverging manner, and both forces can work together on appeared as a co-option to some form(s) of intraspecific different temporal (e.g., juvenile vs. adult life stages) or spatial

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FIGURE 4 | In some aposematic species warning signals are also used for intraspecific communication. (A) In the postman butterfly, Heliconius erato, wing color pattern can serve a dual purpose in predator deterrence and mate attraction; (B) Some wasps can use their facial yellow-and-black markings for individual recognition and status signaling; (C) Males of the dyeing poison frog (Dendrobates tinctorius) tend to have yellower dorsal areas, possibly to enhance protection from predators during tadpole transport, while females with higher amounts of yellow in their frontal area are more often found in courtship; (D) In some populations of the strawberry poison frog (Oophaga pumilio), brighter males are preferred by females and also have a higher status in agonistic encounters with other males. Photos: (A) S. Finkbeiner; (B) E. Florin Niga; (C) B. Rojas; (D) A. Pašukonis.

(e.g., geographic) scales. Depending on the cognitive abilities spent while approaching and courting females of the co-mimic of receivers (predators and mates) signals may be perceived species (Jiggins et al., 2001; Estrada and Jiggins, 2008). Therefore, differently, leading to differential selection and reaching different the multimodal nature of animal signals is prone to the evolution balances between them (Endler, 1992). An example of both forces of complex biological interactions (Maynard Smith and Harper, acting at the same time can be observed in the strawberry poison 2003), yet these are seldom addressed simultaneously. In the frog, Oophaga pumilio, where females have been shown to prefer following sections, we discuss in detail how natural and sexual males with the brightest warning signal (Maan and Cummings, selection can influence aposematic displays. 2008) who, in turn, have the most noxious chemical defense (Maan and Cummings, 2012). This type of “honest signaling” of The Interactive Effect of Natural and prey defenses may facilitate synergistic selection of both warning Sexual Selection Can Maintain Intra-and and sexual signal efficiency (Maan and Cummings, 2012; see details below) as females may benefit from mating with well- Inter-Population Variation in Warning defended males. Coloration When these dual selection pressures work in a divergent The interplay between natural and sexual selection in the manner, sometimes they can cancel each other’s effect or lead evolution of aposematic signals is particularly interesting in to fluctuating evolutionary responses of the warning signal species in which the variability of the signal challenges the depending on the selection strength of each side over time. “uniformity” assumption of aposematism. Whilst a non-variable For example, although under stabilizing selection by predators, signal within a population is expected in order to favor predator female preference has been shown to facilitate phenotypic avoidance learning (Endler, 1988a; Joron and Mallet, 1998; Mallet divergence through hybridization in harlequin poison frogs, and Joron, 1999; Lindström et al., 2001; Endler and Mappes, 2004; Oophaga histrionica (Medina et al., 2013). In Neotropical Darst et al., 2006; Mallet, 2010; Chouteau et al., 2016), as stated longwing butterflies, genus Heliconius, two sister species (H. above, a variable signal–without losing its conspicuous nature- melpomene and H. cydno) have recently diverged to mimic could be associated with the relative attractiveness of some different model taxa, which increases the survival benefits of individuals over others (Ueno et al., 1998; Maan and Cummings, both, but their mimetic coloration could lead to a cost associated 2009). For that reason, aposematic species with a high within- to mate recognition in both species due to the time and energy population phenotypic variability are excellent models to test

Frontiers in Ecology and Evolution | www.frontiersin.org 5 July 2018 | Volume 6 | Article 93 Rojas et al. Aposematic Signals and Mate Attraction how both natural and sexual selection affect the evolution and their frontal area, which is highly visible during courtship design of warning signals. interactions (Rojas, 2012). Pairs in this population show no Among the extensive scientific literature regarding aposematic signs of assortative mating for color patterns, which could species, only a handful of species have been studied in terms help explain the high phenotypic variation observed (Rojas, of how warning signal diversity varies intraspecifically both 2012). within and between populations. Whilst many studies have As with vertebrates, studies aiming to explain warning color expanded our knowledge on the shape and function of warning polymorphism within populations of arthropods are mainly signals, most have focused only on the emitter end (i.e., the focused on frequency-dependent selection (Benson, 1972; Mallet prey). However, to understand the complexity of warning signal and Barton, 1989; Langham, 2004; Borer et al., 2010; Nokelainen variation within and between populations, it is necessary to et al., 2014) or mating preferences (Chouteau et al., 2016). Unlike determine what are the pressures that could be affecting the vertebrates, however, insects have been well-studied at different survival and reproductive success in populations, and how life stages in relation to aposematic signals and their interplay these warning displays act in concert to outweigh the cost of with allelochemical sequestration (Marples et al., 1994; Roque- their expression (Hebets and Papaj, 2005; Gohli and Hogstedt, Albelo et al., 2002), allowing the opportunity to study carry-over 2009). effects of early life on the adult expression of warning coloration One of the species in which multiple selective factors have and chemical defenses. been studied in relation to warning signal evolution, within and Multiples studies have focused on the striking warning between populations, is the strawberry poison frog, Oophaga signal polymorphism observed in some ladybeetles (family pumilio. Several studies have shown that the geographic variation Coccinnelidae). For instance, Osawa and Nishida (1992) and and polymorphism in its aposematic signals is the result of Awad et al. (2015) showed that polymorphism in the elytra the combined action of natural and sexual selection. Predators coloration of Harmonia axyridis is maintained either by seasonal avoid warningly colored plasticine models in the field (e.g., mating variation or assortative mating (respectively; Osawa and Saporito et al., 2007; Hegna et al., 2011), and controlled Nishida, 1992; Awad et al., 2015). In Adalia bipunctata, in experiments in the laboratory have shown that not only do contrast, the polymorphism is maintained by assortative mating females prefer to mate assortatively with males of their own coupled with inheritance of female preference (Majerus et al., morph [Summers et al., 1999; Reynolds and Fitzpatrick, 2007; 1982), showing negative frequency-dependent mating selection Maan and Cummings, 2008; but see Yang et al. (2016) for (i.e., females prefer the rare morph; O’Donald and Majerus, a study showing that assortative mating occurs in allopatric 1984). populations but not in sympatric ones], but also prefer overall Another group in which these two selective pressures have males with brighter coloration (Maan and Cummings, 2009). been widely studied is the Neotropical butterflies of the However, calls (acoustic signals) seem to be more important than genus Heliconius. These butterflies, which occur in Central coloration for female choice (Dreher and Pröhl, 2014). Males and Northern South America, are characterized by wings with hold territories that are defended from other males through conspicuous markings (e.g., yellow, white, red, etc.) on a dark calls, and calling activity and perch height, a proxy for exposure, background, which inform predators about the possession of are correlated with mating success (Pröhl and Hödl, 1999). cyanide compounds that make them toxic (Nahrstedt and Davis, Only the most conspicuous males can afford to use the more 1983; Zagrobelny et al., 2004; Cardoso and Gilbert, 2013). In exposed calling sites (Rudh et al., 2011), as they are presumably this genus, the evolution of distinct color patterns between better protected from predators. More conspicuous or brighter populations has been extensively explained in the context of males are also bolder (Rudh et al., 2013) and more aggressive Müllerian mimicry, in which a warningly colored aposematic (Crothers et al., 2011; Crothers and Cummings, 2015), suggesting species mimics the appearance of another one to share the that aposematic signals in this species have also been co-opted costs of predator education (Müller, 1879). Although both the as an indicator of fighting abilities (Crothers and Cummings, composition and spatial variation of the predator communities 2015). selecting for this resemblance in their coloration are still In the dyeing poison frog, Dendrobates tinctorius, an interplay unknown (Merrill et al., 2015), these mimetic species have between natural and sexual selection affecting warning signals become a textbook example of natural selection (Jiggins, 2017). has also been proposed, although in lesser detail. Field studies However, others studies have also explored how sexual selection, with frog models at Nouragues Reserve (French Guiana) have via mate choice and assortative mating (Jiggins et al., 2001; shown that the warning signals of D. tinctorius elicit few Estrada and Jiggins, 2008; Merrill Richard et al., 2014), has shaped avian predator attacks (Noonan and Comeault, 2009; Rojas wing coloration. For example, in a recent study, Finkbeiner et al. et al., 2014) and are subject, as expected, to positive frequency- (2014) tested the relative importance of color and pattern in dependent selection (Comeault and Noonan, 2011). Males of predation avoidance and mate choice in Heliconius erato. The this population have a higher proportion of yellow in their authors found that although the right combination of local color dorsal area than females, and the authors suggest that a synergy and pattern provided the highest deterrence and mate attraction, between sexual selection (in the form of parental care) and color seemed to be more important than pattern, suggesting that aposematism could select for yellower males (Rojas and Endler, sexual and natural selection work in parallel to influence the 2013). Females, in contrast, seem to be favored by sexual evolution of warning coloration in this species (Finkbeiner et al., selection when they present a higher amount of yellow in 2014).

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Interactive Effects of Natural and Sexual butterflies. The color and pattern of their wings (reviewed in Selection May Lead to Population Jiggins, 2017), coupled to a very characteristic flight behavior Divergence and Speciation (Srygley, 1999), help predators recognize and subsequently avoid them, but the former are also involved in mate recognition. Inter-population variation in multimodal warning signals This suggests that the ultimate fitness of individuals displaying provides an opportunity for unraveling how populations diverge different combinations of these traits is determined by both and, eventually, in some cases, how new species originate. This synergies and compromises between the different functions can also occur through the joint effect of natural and sexual (Merrill et al., 2015). Several of these species belong to local selection on aposematic traits (Maan and Seehausen, 2011). mimicry rings, making their appearance the subject of strong Population divergence through natural selection alone would purifying selection, but also strong assortative mating (Jiggins require extreme combinations of parameters (e.g., almost null et al., 2001). Under these conditions, novel forms are punished by migration and strong selection for ecological specialization) a higher predation due to frequency-dependent selection (Mallet to be fulfilled because gene flow would decrease the level of and Barton, 1989). Hybrids would be expected to have the same diversification (Mayr, 1963). Therefore, the effects of sexual fate if their appearance deviates from the parental phenotype(s) selection are required to promote sexual isolation (through pre- (Merrill et al., 2012); however, one of the most fascinating and post-zygotic mechanisms), together with the effect of linkage aspects of this system is that hybridization has offered a route disequilibrium to maintain the traits correlated and inherited to speciation (Mavárez et al., 2006; Mallet, 2007; Salazar et al., by the following generation (Servedio, 2009). This interplay 2010). Wing color patterns in Heliconius are thus involved in is particularly important for ecological speciation in sympatry, predator deterrence, species recognition, and mating preferences. which occurs when reproductive isolation has evolved as an However, colors can be only one component of a multimodal adaptation to different environments (reviewed in Rice and mating signal that also involve chemical components, e.g., Hostert, 2017), or through hybridization, which can generate pheromones. Even in a community consisting of mimetic species, novel traits capitalizing on existing variation between related visual attraction can be based at first on wing appearance, yet ata species (Mallet, 2007; Salazar et al., 2010). Additionally, the shorter range scents from the wings and the genitalia can provide relaxation of predation pressure on aposematic species leaves species-specific chemical signatures leading to assortative mating room for traits to be selected by sexual selection, especially if (Mérot et al., 2015). predators associate these mating signals with unprofitability. As seen in the previous section, poison frogs (family Chemical Compounds Can Play a Role in Dendrobatidae) can use warning coloration as a mating signal. However, the predominant modality of anuran mating signals Mate Attraction and Predator is acoustic (i.e., advertisement calls). A recent study by Santos Deterrence—But Could They Also Have a et al. (2014) demonstrated that acoustic mating signals in Dual Function? poison frogs (Dendrobatidae) have diversified in association Insects offer a prime example of sexual communication mediated with aposematism due to sexual selection, such that aposematic by chemical signals such as pheromones. As such, the divergence species have calls with a set of characteristics that differ from in pheromone components has shown to play a key role also in those of non-aposematic species (Santos et al., 2014). The speciation (Groot et al., 2006, 2009). Pheromone composition level of conspicuousness in different populations of O. pumilio and variability have been studied in detail in bella moths, also predicts other aspects of the sexual display behavior, with Utheteisa ornatrix (Conner et al., 1981), moths in the genus males from more conspicuous populations calling from more Heliotis (Klun et al., 1980; Teal et al., 1984; Heath et al., 1991) and exposed sites (Pröhl and Ostrowski, 2011; Rudh et al., 2011), bark beetles (genus Ips; Lanier et al., 1980; Seybold et al., 1995). and being more aggressive and explorative (Rudh et al., 2013). As well as long-range pheromones, cuticular hydrocarbons (or These behavioral differences coupled with mechanisms such as CHCs) have also been shown to play an important role in assortative mating could generate pre-zygotic isolation leading intraspecific communication and mate choice in insects (Sharma to population divergence, in the first place, and potentially to Manmohan et al., 2011; Ingleby, 2015). a speciation process in the long term. Indeed, in O. pumilio, The use of defensive chemicals is also widespread throughout molecular approaches show that color, but not body size, is insects. In addition to their crucial role in predator deterrence, diverging at high rates, indicating selection (Wang and Shaffer, a linkage between defensive chemicals and intraspecific 2008; Brown et al., 2010). Moreover, these studies demonstrate communication has been shown in many insect species. For that sexual and natural selection are causing genetic isolation instance, in Lepidoptera, different families (e.g., Nymphalidae, between different color morphs in the wild, which could be Danaidae, and Erebidae) use secondary compounds such as a sign of incipient speciation (Wang and Summers, 2010). pyrrolizidine alkaloids in male courtship displays, nuptial gifts, This is supported by recent findings showing that, within and egg protection (Boppré et al., 1978; Brown, 1984; Moore Dendrobatidae, the aposematic lineages are speciating at higher et al., 1990; Weller et al., 1999). For example, males of U. ornatrix, rates than their non-aposematic counterparts (Santos et al., have glandular structures in which they store pyrrolizines. Males 2014). unable to produce certain compound derived from these The synergistic effects of sexual selection and natural selection alkaloids have been found to be less successful at courting are also likely to affect speciation processes in Heliconius females (Conner et al., 1981). In fact, it has been suggested that

Frontiers in Ecology and Evolution | www.frontiersin.org 7 July 2018 | Volume 6 | Article 93 Rojas et al. Aposematic Signals and Mate Attraction this compound is used by females to assess the extent to which Because taking the first (or last) articles in the search list the male is chemically protected (Conner et al., 1981). A similar would have constrained the timeframe, we took the first 10% example can be found in the beetle Neopyrochroa flabellate of the number of articles published each year, which varied (Eisner et al., 1996a,b). between 10 in 1990 and 87 in 2017 (Figure 5), that fitted the However, we currently have very little information on whether following criteria. We only included articles studying an actual sexual selection and natural selection shape the secondary natural animal system (i.e., no plants), and assessing directly or defenses synergistically. In some aposematic species, levels indirectly the effect of natural (predation) and/or sexual selection of secondary defense have shown to differ between females in the signals considered. Therefore, studies done with artificial and males at the reproductive life-stage, which may suggest prey represented as symbols or using artificial chemicals were differential selection. For example, burying beetles (Nicrophorus excluded. Artificial prey were accepted if they aimed to represent vespilloides) use their anal exudates both for their own defense the actual animal studied, as in dummies or models. We also and the protection of their offspring, and females appear to excluded taxonomic descriptions, as well as phylogenetic and produce more of these exudates than males (Lindstedt et al., phylogeographic studies in which there was no direct relation 2017). Allocation for chemical defense has also shown to with the selection pressures on which we focus this review. For trade off with reproductive success indicating that these two each paper we recorded the focal species identity, the trait(s) functions could play important role in both mate attraction and studied, whether or not they consider the multimodality aspect, predator deterrence (Nokelainen et al., 2012). This interaction and the type of selection addressed (Table 1). is further complicated by the fact that many species sequester As revealed by our search, aposematism is a phenomenon their chemical defenses from their diet. In the true bug Lygaeus that has raised increasing interest among researchers over equestris, for example, diet, and therefore level of chemical the last three decades (Figure 5), and has been studied in a defense, has no effect on mate choice (Burdfield-Steel et al., variety of organisms (Figure 3), spanning gastropods through 2013). This is despite evidence that females of this species pass to carnivores. Nevertheless, invertebrates seem to be studied defensive chemicals on to their eggs, protecting them from more, in ∼69% of the cases (Figure 6A); perhaps not surprising predators (Newcombe et al., 2013). When variation between considering they cover 97% of organisms on earth. Both individuals is purely environmental, effects on mate choice may within invertebrates and vertebrates, there are taxonomic groups only occur when direct benefits are high (as in several of the accounting for the majority of the studies (Figure 6A). Among examples given above), although see (Geiselhardt et al., 2012) for invertebrates, the best studied are lepidopterans (34.2%), such an example of diet and host plant leading to associative mating as longwings (5.7%), coleopterans (20.5%), and other insects based on CHC (cuticular hydrocarbons) profile. When direct (34.2%). Among vertebrates, poison frogs are undoubtedly the benefits are low, species in which chemical defense level is either group that has stimulated most research (68.9%), followed by genetically determined, or indicative of overall quality, may be snakes (18.2%; Figure 6A). better candidates in which to look for mate choice based on Regardless of the taxonomic group, most studies have focused defense level. This may well be the case in species that produce on unimodal signals, particularly visual (59.4%), and chemical their defenses de novo. (16%; Figure 6B). Multimodal signals were studied only in 17.9% of the cases, and consisted in all cases of visual signals in

MOVING TOWARD A MORE INTEGRATED VIEW OF APOSEMATIC SIGNALS

Despite all the examples discussed so far, it is clear that only a few studies address how both natural and sexual selection act (either synergistically or antagonistically) on the evolution of multimodal aposematic signals. Furthermore, it is apparent that not only color, but also odor, taste, and behavior are part of warning displays, and their interaction, besides strengthening the signal, can provide reliable information about the quality of the emitter. Yet, only a handful of studies have considered the interplay among these, and their joint significance remains barely tested. To corroborate these impressions, we conducted a literature search in Web of Science and analyzed the contents of a representative sample of the articles available on aposematism. We used the search terms “aposematism or aposematic” to have the widest spectrum possible of studies and organisms, and limited the search to articles published in or after 1990 and until mid-April 2018. This search rendered a total of 1,051 articles, out FIGURE 5 | The number of studies on aposematism has been increasing over the last three decades. See text for details on data used. of which we analyzed 105 (10%) selected as explained below.

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TABLE 1 | Studies included in the review of literature published on aposematism over the last three decades.

Year Organism Common name Higher classification Selection pressur Trait(s) References addressed studied

2018 Pseudophryne spp Australian brood frogs Anura pred col Lawrence et al. 2018 Nudibranchs Sea slug Gastropoda pred chemdef Winters et al. 2018 Andinobates bombetes Poison frog Anura pred col Casas-Cardona et al. 2017 Vipera seoanai Iberian cross adder Squamata pred col+patt Martínez-Freiria et al. 2017 Nicrophorus Burying beetle Coleoptera both col+chemdef Lindstedt et al. vespilloides 2017 Oophaga pumilio Strawberry poison frog Anura pred col+patt Preissler and Pröhl 2017 Arctia plantaginis Wood tiger moth Lepidoptera pred chemdef Rojas et al. 2017 Danainae Milkweed butterfly Lepidoptera pred col Aluthwattha et al. 2017 Pyrrhocoris apterus Firebug Hemiptera pred col Landova et al. 2017 Nudibranchs Sea slug Gastropoda pred col+chemdef Winters et al. 2017 Pyrrhocoris apterus Firebug Hemiptera pred col Benes and Vesely 2017 Heliconius Longwings, heliconians Lepidoptera both col+patt Chouteau et al. 2016 Heliconius Longwings, heliconians Lepidoptera pred chemdef Arias et al. 2016 Bombus Bumblebee Hymenoptera pred sound Moore and Hassle 2016 Arctia plantaginis Tiger moth Lepidoptera both col Lindstedt et al. 2016 Oophaga pumilio Strawberry poison frog Anura ss col Gade Et al. 2016 Heliconius Longwings, heliconians Lepidoptera pred col Dell’Aglio et al. 2016 Pyrrhocoris apterus Firebug Hemiptera pred col Adamova-Jezova et al. 2016 Lampyridae Firefly Coleoptera pred chemdef Vencl et al. 2015 Indian butterflies Other butterfly Lepidoptera both col Su Et al. 2015 Arctia plantaginis Wood tiger moth Lepidoptera pred pattern Honma et al. 2015 Arctia plantaginis Wood tiger moth Lepidoptera both col Gordon et al. 2015 Adalia bipunctata Two-spotted ladybird Coleoptera both chemdef Paul et al. 2015 Pyrrhocoris apterus Firebug Hemiptera pred col Exnerova et al. 2015 Dendrobates inctorius Dyeing poison frog Anura pred col+patt Hämäläinen et al. 2014 Euphydryas and Other butterfly Lepidoptera pred col+chemdef Long et al. Chlosyne 2014 Heliconius erato Longwings, heliconians Lepidoptera both col+patt Finkbeiner et al. 2014 Paederus fuscipes Rove beetle Coleoptera pred chemdef Tabadkani and Nozari 2014 Dendrobates tinctorius Dyeing poison frog Anura pred col+patt Rojas et al. 2014 Arctia plantaginis Wood tiger moth Lepidoptera pred pattern Hegna and Mappes 2014 Oophaga pumilio Strawberry poison frog Anura pred col+patt Qvarnström et al. 2014 Oophaga granulifera Strawberry poison frog Anura pred col Willink et al. 2013 Rana rugosa Japanese wrinkled frog Anura pred chemdef Yoshimura and Kasuya 2013 Oophaga histrionica Harlequin poison frog Anura ss col Medina et al. 2013 Oophaga granulifera granular poison frog Anura pred col Willink et al. 2013 Heteroptera True bugs Hemiptera pred col Svadova et al. 2013 Oophaga pumilio, Strawberry poison frog, granular Anura both col+sound Pröhl et al. Oophaga granulifera poison frog 2013 Flabellina iodinea Sea slug Gastropoda pred chemdef Noboa and Gillette 2013 Oophaga pumilio Strawberry poison frog Anura pred col Hegna et al. 2012 Heliconius Longwings, heliconians Lepidoptera pred col+patt Merrill Et al. 2012 Oophaga pumilio Strawberry poison frog Anura pred col Stuart et al. 2012 Polistes dominula European paper wasp Hymenoptera pred col+chemdef Vidal-Cordero et al.

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TABLE 1 | Continued

Year Organism Common name Higher classification Selection pressur Trait(s) References addressed studied

2012 Vipera spp. European vipers Squamata pred col+patt Valkonen et al. 2012 True bugs True bugs Hemiptera pred chemdef Noge et al. 2011 Ranitomeya imitator Mimic poison frog Anura pred col Chouteau and Angers 2011 Lycorma delicatula Spotted lanternfly Hemiptera pred col Kang et al. 2011 Motyxia spp Millipede Myriapoda pred luminescence Marek et al. 2011 Oophaga pumilio Strawberry poison frog Anura both col Ozel and Stynoski 2011 Cynops pyrrhogaster Japanese fire belly newt Caudata pred col Mochida 2010 Oreina gloriosa Leaf beetles Coleoptera pred col Borer et al. 2010 Graphosoma lineatum Shield bugs Hemiptera pred col Johansen et al. 2010 Bombus spp Bumblebee Hymenoptera pred col Stelzer et al. 2010 Pyrrhocoris apterus Firebug Hemiptera pred col+size Prokopova et al. 2010 Opistobranchs Sea slug Gastropoda pred col+chemdef Cortesi and Cheney 2010 Hypselodoris Sea slug Gastropoda pred col+chemdef Haber et al. fontandraui 2009 Oophaga pumilio Strawberry poison frog Anura ss col Maan and Cummings 2009 Mephitis mephitis Skunk Carnivora pred col+shape Hunter 2009 Photinus Firefly Coleoptera pred luminescence Moosman et al. 2009 Ladybirds Ladybird Coleoptera pred pattern+shape Dolenska et al. 2009 Tiger moths Tiger moth Lepidoptera pred sound Barber et al. 2008 Tiger moths Tiger moth Lepidoptera pred col+sound Ratcliffe and Nydam 2008 Oophaga pumilio Strawberry poison frog Anura ss col Maan and Cummings 2008 Carabid beetles Ground beetle Coleoptera pred col+chemdef Bonacci et al. 2008 Lycidae beetles Net-winged beetle Coleoptera pred chemdef Eisner et al. 2007 Oophaga pumilio Strawberry poison frog Anura pred col Saporito et al. 2007 Cirriformia punctata Polychaete Polychaeta pred chemdef Meredith et al. 2007 Oophaga pumilio Strawberry poison frog Anura ss col Reynolds and Fitzpatrick 2007 Harmonia axyridis Asian ladybeetle Coleoptera pred col+chemdef Bezzerides et al. 2007 Tiger moths Tiger moth Lepidoptera pred sound Barber and Conner 2006 Micrurus phyrrocryptus Coral snake Squamata pred colpatt Buasso et al. 2006 Carabid beetles Ground beetle Coleoptera pred col+chemdef Bonacci et al. 2006 Graphosoma lineatum Shield bugs Hemiptera pred col+chemdef Veseley et al. 2006 Pyrrhocoris apterus Firebug Hemiptera pred col Exnerova et al. 2005 Cycnia tenera Tiger moth Lepidoptera pred sound Ratcliffe and Fullard 2005 Vipera berus Common European adder Squamata pred pattern Niskanen and Mappes 2005 Ensatina eschscholtzii Lungless salamander Caudata pred col Kuchta xanthoptica 2004 Vipera berus Common European adder Squamata pred pattern Wüster et al. 2004 Heliconius Longwings, heliconians Lepidoptera pred col+patt Langham 2004 Oophaga pumilio Strawberry poison frog Anura both col Siddiqi et al. 2003 Poison frogs Poison frog Anura pred col+size Hagman and Forsman 2003 Poison frogs Poison frog Anura pred col+chemdef Santos et al.

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TABLE 1 | Continued

Year Organism Common name Higher classification Selection pressur Trait(s) References addressed studied

2003 Vespula norwegica Norwegian wasp Hymenoptera pred col+shape Kauppinen and Mappes 2002 Eumaeus minyas Lycaenid butterfly Lepidoptera pred chemdef Castillo-Guevara and Rico-Gray 2002 Murgantia histrionica Harlequin bug Hemiptera pred chemdef Aliabadi et al. 2001 Pseudoxycheila tasalis Neotropical tiger beetle Coleoptera pred col Schultz 2001 Pseudoxycheila tasalis Neotropical tiger beetle Coleoptera pred chemdef Schultz and Puchalski 2000 Cercopidae Froghopper Hemiptera pred col+chemdef Peck 2000 Schistocerca gregaria Desert locust Orthoptera pred col+chemdef Sword et al. 1999 Cosmopepla Stink bug Hemiptera pred chemdef Krall et al. bimaculata 1999 Nudibranchs Sea slug Gastropoda pred col Giménez- Casalduero et al. 1999 Bombus terrestris Buff-tailed bumblebee Hymenoptera pred sound Kirschner and Roschard 1998 Romalea guttata Lubber grasshopper Orthoptera pred col+behav Hatle and Faragher 1998 Flatworms Flatworms Platyhelminthes pred col Ang and Newman 1997 Ithomiine and tiger Tiger moth Lepidoptera pred chemdef Cardoso moths 1996 Neotropical butterflies Neotropical butterflies Lepidoptera pred col+behav Pinheiro 1996 Mephitis mephitis Striped skunk Carnivora pred sound+behav Lartviere and Messier 1995 Tiger moths Tiger moth Lepidoptera pred sound Dunning and Kruger 1995 Coral snakes Coral snake Squamata pred col+patt Brodie and Janzen 1994 Coccinella Seven-spot ladybird Coleoptera pred col+chemdef Marples et al. septempunctata 1994 Opistobranchs Sea slug Gastropoda pred col+chemdef Tullrot 1993 Catocala spp Underwing moths Lepidoptera pred col Ingalls 1993 Monistria concinna Grasshopper Orthoptera pred col+chemdef Groeters and Strong 1992 Tiger moths Tiger moth Lepidoptera pred sound Dunning et al. 1991 Polycera quadrilineata Sea slug Gastropoda pred col Tullrot and Sundberg 1991 Leaf beetles Leaf beetle Coleoptera pred chemdef Pasteels and Rowellrahier 1990 Battus philenor Blue swallowtail Lepidoptera pred col Codella and Lederhouse

See main text for details on inclusion criteria. pred, predation; ss, sexual selection; col, color; patt, pattern; chemdef, chemical defenses. References in chronological order (from oldest to newest): (Codella and Lederhouse, 1990; Pasteels and Rowellrahier, 1991; Tullrot and Sundberg, 1991; Dunning et al., 1992; Groeters and Strong, 1993; Ingalls, 1993; Marples et al., 1994; Tullrot, 1994; Brodie and Janzen, 1995; Dunning and Kruger, 1995, 1996; Lartviere and Messier, 1996; Pinheiro, 1996; Cardoso, 1997; Ang and Newman, 1998; Hatle and Faragher, 1998; Gimenez-Casalduero et al., 1999; Kirchner and Roschard, 1999; Krall et al., 1999; Peck, 2000; Sword et al., 2000; Schultz, 2001; Schultz and Puchalski, 2001; Aliabadi et al., 2002; Castillo-Guevara and Rico-Gray, 2002; Kauppinen and Mappes, 2003; Santos et al., 2003; Langham, 2004; Siddiqi et al., 2004; Wuster et al., 2004; Kuchta, 2005; Niskanen and Mappes, 2005; Bonacci et al., 2006, 2008; Buasso et al., 2006; Exnerová et al., 2006, 2015; Vesely et al., 2006; Barber and Conner, 2007; Bezzerides et al., 2007; Meredith et al., 2007; Reynolds and Fitzpatrick, 2007; Saporito et al., 2007; Eisner et al., 2008; Maan and Cummings, 2008, 2009; Ratcliffe and Nydam, 2008; Barber et al., 2009; Dolenska et al., 2009; Hunter, 2009; Moosman et al., 2009; Borer et al., 2010; Cortesi and Cheney, 2010; Haber et al., 2010; Johansen et al., 2010; Prokopova et al., 2010; Stelzer et al., 2010; Chouteau and Angers, 2011; Kang et al., 2011; Marek et al., 2011; Mochida, 2011; Ozel and Stynoski, 2011; Pröhl and Ostrowski, 2011; Merrill et al., 2012; Noge et al., 2012; Stuart et al., 2012; Valkonen et al., 2012; Vidal-Cordero et al., 2012; Hegna et al., 2013; Medina et al., 2013; Noboa and Gillette, 2013; Pröhl et al., 2013; Svadová et al., 2013; Willink et al., 2013, 2014; Yoshimura and Kasuya, 2013; Finkbeiner et al., 2014; Hegna and Mappes, 2014; Long et al., 2014; Qvarnström et al., 2014; Rojas et al., 2014, 2017; Tabadkani and Nozari, 2014; Gordon et al., 2015; Hämäläinen et al., 2015; Honma et al., 2015; Su et al., 2015; Adamova-Jezova et al., 2016; Arias et al., 2016; Dell’aglio et al., 2016; Gade et al., 2016; Lindstedt et al., 2016, 2017; Moore and Hassall, 2016; Vencl et al., 2016; Aluthwattha et al., 2017; Benes and Vesely, 2017; Chouteau et al., 2017; Landová et al., 2017; Martinez-Freiria et al., 2017; Preissler and Pröhl, 2017; Winters et al., 2017, 2018; Casas-Cardona et al., 2018; Lawrence et al., 2018).

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combination with either chemical defenses (15.1%) or auditory signals (2.8%; Figure 6B). Not surprisingly, most studies on aposematism have addressed either directly or indirectly the effect of natural selection (predation) on the studied signals. As pointed out above, however, there is an increasing interest in systems or contexts in which the effect of both natural and sexual selection can be studied simultaneously. Of all the studies reviewed, only 4.7% addressed exclusively the effect of sexual selection on warning signals, while 9.4% investigated the effects of both selective forces jointly (Figure 6C). Most importantly, studies in which the effects of natural and sexual selection are investigated at the same time tend to focus only on one sensory modality, in particular the visual, even if two components of a signal, for example color and pattern, are taken into account. This tendency seems to be as true for vertebrates, as it is for invertebrates (Figure 7). Studies addressing the influence of predation on multimodal signals seem to be slightly more common in invertebrates than in vertebrates (Figure 7). This is most likely because insects, the invertebrate group most studied in this context, can be more easily bred and kept in the laboratory due to their short- generation times and numerous offspring, and studied under manipulated conditions. Moreover, in many cases it is easier to disentangle the visual and chemical components of their multimodal warning displays (Marples et al., 1994; Rönkä et al., 2018a,b). Most importantly, the overrepresentation of some groups in these studies may be partially due to the dynamics of predator-prey coevolution and the speed to respond to selection (Härlin and Härlin, 2003). These may favor aposematism in organisms such as insects, amphibians, or reptiles, which lean toward an r-strategy (numerous offspring, high growth rate and low per capita probability of survival), while constraining it in organisms such as mammals and birds, which lean toward a K-strategy (few offspring, low growth rate and high per capita probability of survival), and are more often the selective agents. To investigate this further, not only do we need new model species with well-studied visual signals and chemical communication, but also where the traits in question are heritable, and known to be under identified selective pressures (i.e., predation and sexual selection). Here, we propose the wood tiger moth, A. plantaginis, as one of such emerging model species where multimodal warning displays can be studied while addressing conflictive or synergistic selective pressures, as stated below.

THE WOOD TIGER MOTH AS A PROMISING MODEL TO STUDY MULTIMODALITY IN APOSEMATIC AND FIGURE 6 | (A) Representative animal groups studied in relation to aposematism over the last three decades. The larger the area, the more SEXUAL SIGNALING studies on that particular group. (B) Signaling modalities studied in relation to aposematism over the last three decades. The larger the area, the more One of the species in which multimodal aposematic signals have studied. (C) Selection pressures taken into account in studies on been studied in depth is A. plantaginis (formerly Parasemia aposematism over the last three decades. The larger the area, the more plantaginis; Rönkä et al., 2016), the wood tiger moth (Figure 8). studies taking that particular selective pressure into account. A. plantaginis is an aposematic diurnal moth with a widespread

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FIGURE 7 | Number of studies that address the effects of predation, sexual selection, or both on one (unimodal) or two (multimodal) signals in the aposematic displays of (A) invertebrates, and (B) vertebrates.

FIGURE 8 | The different morphs of the wood tiger moth in Europe. The upper row shows polymorphic color variation in males, whereas the bottom row showcases the continuous variation observed in females. Reproduced with permission from Nokelainen (2013). Photos: S. Waldron. geographic distribution across the holarctic region (Hegna et al., second is targeted toward avian predators (Rojas et al., 2017) and 2015). Larvae of this species are polyphagous, feeding on a large contains pyrazines, which the moths produce de novo (Burdfield- number of different genera (Ojala et al., 2005), and overwinter at Steel et al., 2018), likely on the basis of constituents obtained from their 4th−5th instar. The adult stage lasts for about 2–3 weeks their diet. These defenses are advertised to birds with brightly during which these moths do not feed. This means that both colored hindwings, where red, yellow, or even white coloration their coloration and chemical defenses are set at the larval stage is contrasted with black patterning (Figure 8). (Ojala et al., 2005). Males spend their adult life flying in search of females, who are ready to mate soon after eclosion. While their coloration has been shown to have a strong Predation Is a Strong Selective Pressure hereditary component (Nokelainen et al., 2013; Lindstedt et al., on Wood Tiger Moth Warning Coloration 2016), diet can also influence adult coloration, particularly in and Chemical Defenses females (Lindstedt et al., 2010; Furlanetto, 2017; Figure 9). Surprisingly, given their role in predator deterrence, the In addition, their chemical defenses are affected by resource hindwings of wood tiger moths show considerable color availability during early life (Brain, 2016; Furlanetto, 2017; variation, both within and between populations (Hegna et al., Figure 9). As the moths are most active during daylight hours 2015; Figure 8). In the Finnish population, which has been (Rojas et al., 2015a) they are vulnerable to predation by birds, the focus of much of the research on this species, males show particularly while resting on the vegetation, where they are discrete color polymorphism, possessing either white or yellow clearly conspicuous (Nokelainen et al., 2012; Henze et al., 2018). hindwings, while females vary continuously from yellow to red. Likewise, they can be vulnerable to attacks by invertebrate In contrast, in the putative ancestral populations (Caucasus) predators, especially when the temperature is not high enough males exhibit continuous variation from yellow-orange through for the moth to initiate flight, or when it is eclosing from the to red in their hindwing coloration, while females display red pupa and its wings are not yet fully extended. Adult moths defend hindwings. The forewings, on the other hand, do not vary much themselves with two distinct defensive fluids, one produced from within populations, and consist of high-contrast black and white the anal tract and one from glands behind the head (Figure 9). patterning. Many studies to date have demonstrated the predator- The first is targeted toward invertebrate predators, while the deterrent nature of this moth’s coloration (Lindstedt et al., 2011;

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FIGURE 9 | A schematic illustration of the different selective (dark) and environmental (light) factors currently known to be acting on chemical (green) and visual (blue) signals in the wood tiger moth. Anti-clockwise from top left: (A) Female neck defensive fluids are deterrent to avian predators; (B) Female melanisation is heritable and influenced by larval diet; (C) Female hindwing coloration is highly heritable, affected by larval diet, and influences avian predation risk; (D) Males follow female pheromone trails; (E) Male abdominal defensive fluids deter invertebrate predators; (F) Male hindwing colouration is heritable and plays a role in both predator deterrence and male mating success; (G) Male melanisation is heritable and influences both thermoregulation and predation risk; (H) Male neck defensive fluids are deterrent to avian predators. See text for details.

FIGURE 10 | Caucasian populations of the wood tiger moth are characterized by the lack of sexual dimorphism in hindwing colouration seen in Europe. In Georgia, both males (A) and females (B) exhibit hindwing coloration rich in long wavelengths resulting in continuous red-orange coloration. Photos: B. Rojas.

Nokelainen et al., 2012, 2014; Hegna and Mappes, 2014) and, efficient chemical defenses against ants, and a more repulsive lately, the same has been shown for its chemical defenses, even odor against avian predators when presented in isolation from when experimentally decoupled from the visual signals (Brain, the visual signal (Rojas et al., 2017), although the fluids of both 2016; Rojas et al., 2017). morphs seem to be unpalatable even when presented in the Male multimodal warning display has been shown to have absence of color cues. When the warning colors are presented to important consequences for predator defense. A series of birds in association with the natural chemical defenses (the moth experiments using artificial moths showed that white males as a whole), however, white moths elicit more beak cleaning in suffer higher predation rates in the field when compared to great tits than yellow moths, and are also eaten less when attacked yellows (Nokelainen et al., 2014). Furthermore, when live moths for the first time (Rönkä et al., 2018b). Thus, while yellow males were presented to birds, yellow males elicited longer attack seem to rely mostly on their warning color and repulsive odor to latencies, suggesting yellow males possess stronger warning avoid being attacked, white males seem to rely on taste-rejection signals (Nokelainen et al., 2012). Yellow males seem to have more by predators, indicating that the multiple components of these

Frontiers in Ecology and Evolution | www.frontiersin.org 14 July 2018 | Volume 6 | Article 93 Rojas et al. Aposematic Signals and Mate Attraction moths’ warning displays repel wild-caught predators at different of the flying and maneuvering while searching for females. These stages of predation. Furthermore, white and yellow male color ecological and behavioral differences between the sexes make it morphs trade-off between efficient warning and sexual signaling likely that the optimal values of signaling and defenses against (see below). The white-colored males generally have a higher predators are not the same for females and males. mating success (Nokelainen et al., 2012; Gordon et al., 2015) Although natural selection can work on sexually dimorphic whereas the yellow-colored males are more avoided by avian signals, and can both restrict or enhance the evolution of predators (Nokelainen et al., 2012). Moreover, changes in the differences between sexes, sexual selection has been put forward composition of the avian predator community can influence the as the main driving force of sexual dimorphism in Lepidoptera direction of signal selection (Nokelainen et al., 2014), which, (Shine, 1989; Allen et al., 2010). A recent study examining combined with spatial variation in differential mating success, the visual capabilities of both male and female wood tiger may operate as a selection mosaic whereby dispersal facilitates moths indicated that these moths are unable to distinguish the maintenance of genetic (Galarza et al., 2014), and hence among the different shades of orange-red that a female could phenotypic variation (Gordon et al., 2015). have in its hindwings (Henze et al., 2018); this suggests that Females are also well protected from predation. They, too, female coloration, as well as the coloration of Caucasian males, produce chemical defenses that deter birds effectively, but are is unlikely to be influenced by sexual selection. Females, in costly to produce (Brain, 2016; Furlanetto, 2017). Red females contrast, are capable of distinguishing between the yellow and are slightly more conspicuous (Lindstedt et al., 2011; Henze et al., white coloration of Finnish male hindwings (Henze et al., 2018), 2018), and less frequently attacked by avian predators (Lindstedt pointing at a possible role of sexual selection, perhaps via female et al., 2011) than orange ones, and experiments with wild-caught choice, on male hindwing polymorphism. Interestingly, some birds have demonstrated that the red coloration is learned faster studies have revealed differences between the two male morphs than white and yellow (Rönkä et al., 2018a). in mating success, with white males getting a mating advantage, particularly when more abundant (Gordon et al., 2015) or when Why Are the European Forms Sexually males are stressed/have costs imposed upon them (Nokelainen et al., 2012). Altogether, this hints at a role of coloration in mate Dimorphic? The Emerging Role of Sexual choice or attraction, providing a possible explanation to wood Selection tiger moths’ sexual dimorphism in coloration. Sexual dimorphism, as well as sex-limited mimicry, are highly Ongoing and future work including the investigation of the derived characters in many Lepidopteran systems (Kunte, 2008; genetic mechanisms limiting the genetic correlation between Allen et al., 2010), but do occur multiple times in the Arctiinae. sexes (e.g., sex-limited expression of autosomal genes can However, in Arctiina, the clade to which A. plantaginis belongs facilitate sexual dimorphism; Traut et al., 2007), quantifying (Rönkä et al., 2016), sexual dimorphism is rare, suggesting costs and condition-dependence of sexually dimorphic traits and that the ancestral state of the wood tiger moth is sexually measuring natural and sexual selection in natural populations in monomorphic. Although the putative ancestral (Caucasian) the wood tiger moth system will continue to clarify the roles of forms of the species, as well as closely related species, exhibit a both sexual and natural selection in the origins and maintenance rather reddish coloration in both sexes (i.e., this population is of sexual dimorphism and male polymorphism. not strictly sexually dichromatic; Rönkä et al., 2016; Figure 10), in a great portion of its range wood tiger moth morphs exhibit Components of Chemical Defenses Could sexually dimorphic coloration (Hegna et al., 2015). Moreover, in several European populations white and yellow hind-winged Have a Dual Function in Predator males coexist locally, while females exhibit coloration that varies Deterrence and Mate Attraction continuously from yellow through to orange and red. Recent developments concerning the chemical defenses of Differences in reproductive allocation between males and the wood tiger moth have revealed the presence of two females, and the subsequent differences in mate-searching methopyraxines (2-sec-butyl-3-methoxypyrazine and 2-isobutyl- behavior, can lead to differential exposure of the two sexes to 3-methoxypyrazine) that have a key role in predator deterrence predation. Female wood tiger moths, like many Lepidopteran (Rojas et al., 2017; Burdfield-Steel et al., 2018). By contrast, females, allocate more resources to reproduction than to flight, despite luring A. plantaginis males to pheromone traps during eclosing with eggs ready to be fertilized. As is typical for moths, every field season, our knowledge of the compounds present females use pheromones to attract males, who fly long distances in the pheromone blend(s) of A. plantaginis is only incipient in search of mates. Not surprisingly, males show their activity (Muraki et al., 2017), with a number of microcompounds peak at the same time as the peak in female pheromone calling amongst the most prominent components. Pyrazines have been (Rojas et al., 2015a). Once they detect a female in the distance, found in the pheromone blends of some insects, and seem they follow the pheromone source with a characteristic zig-zag to be particularly common in tiger moths (Rothschild et al., flight. During the last stage of approach, it is also possible that 1984; Guilford et al., 1987; Moore et al., 1990). Thus, we males can detect the females visually, as these are particularly cannot dismiss the possibility that these methopyraxines, or conspicuous against the vegetation on which they rest and call some other compounds found in the prothoracic defensive (Henze et al., 2018). Indeed, male eyes are more sensitive (Henze fluids of these moths, have a dual role in protection from et al., 2018), which makes sense considering that they do most predators and mate attraction. Furthermore, we know that males

Frontiers in Ecology and Evolution | www.frontiersin.org 15 July 2018 | Volume 6 | Article 93 Rojas et al. Aposematic Signals and Mate Attraction transfer a spermatophore to females during mating (Chargé et al., pyrazines could be better protected against predators, which in 2016), but we currently do not know whether some protective turn would inform females that he has the right condition to chemicals, or any other type of nuptial gift, are also transmitted afford the costs of production or sequestration and thus make during this transfer. him more attractive as a mate. To our knowledge, this has been Studies on the interaction between warning coloration and studied in detail only in, U. ornatrix (González et al., 1999; chemical defenses in the context of sexual selection are the next Iyengar and Starks, 2008); see section “Chemical Compounds logical steps in studies on wood tiger moths. They are an excellent Can Play a Role in Mate Attraction and Predator Deterrence— model to test these different components because it is possible But Could They Also Have a Dual Function?” above). Another to test the effect of each in isolation to understand its function way in which sexual and natural selection could act in synergy and importance. The amount of both methoxypyrazines can be on chemical compounds is through the so-called nuptial gifts. A measured from individual moths, allowing detailed estimates of male could, for example, donate defensive chemicals to the female chemical defense level. With our increasing knowledge of the during mating to provide protection for the eggs or herself. In pheromones of this species we can begin to look for links between this type of situation the “odor” of the male could function both pheromone composition and chemical defense, and in particular, as a warning signal for predators and as a signal of mate quality if the resource allocation patterns seen in coloration and defense for the females. Therefore, future research should consider the (Furlanetto, 2017), extend to pheromone production. In that potential synergistic (or opposing) interactions between sexual respect, it is also important to discover whether males produce selection and predation acting simultaneously on chemical and pheromones, as is the case in some butterflies (Darragh et al., visual communication. We can start by investigating if the same 2017) and other day-flying moths (Sarto I Monteys et al., 2016), compounds in the chemical defenses are also present in the and whether those are relevant for female choice/acceptance. If pheromone blends, and how are they then potentially transferred males do have pheromones, it would be key to examine whether to the spermatophores and eggs. We also need to test the there are additive effects of pheromone blend and hindwing relationship between the levels/types of defensive toxins a male color, or whether one signal is more important than the sum possesses, combined with their attractiveness as a mate and of both for mate attraction/choice. The same question could be their defensive coloration. Potentially good model organisms addressed in the context of population divergence, for instance from which we already have information both on the influence to understand if potential variation in the pheromone blends and of sexual and natural selection on different components of chemical defenses link to the differences in coloration between multimodal signals are listed in Table 1. the European and Caucasian populations. 2. Defensive chemicals often evolve under multiple selection, protecting simultaneously from predators, pathogens, and parasitoids (Johnson Pieter et al., 2018). Many chemical CURRENT KNOWLEDGE GAPS AND compounds used in secondary defense or chemical FUTURE DIRECTIONS communication can be sequestered directly from the diet or produced with the help of symbionts, which can alter the As our review shows, previous studies have been focusing chemical profile of their hosts (Engl and Kaltenpoth, 2018). on understanding how sexual or natural selection (seldom However, experimental evidence illustrating these interactions both; Table 1, Figure 6C) could shape the evolution of warning and their effect on host behaviors are still scarce. This is coloration due to its multiple function as a signal of mate quality particularly true for symbionts involved in the production of and possession of chemical defenses. Our review also highlights insect pheromones (Engl and Kaltenpoth, 2018), thus providing the need to study a greater variety of “non-model” species, such a promising research avenue. as the wood tiger moth. In particular, species that possess key 3. It is ideal to investigate the patterns of inheritance of the components such as chemical or visual, may help fill critical gaps signals of interest. If the trait in question is not heritable, there in our existing knowledge. We describe some of these gaps below, are no grounds for natural selection to act on it (even if the and propose some future avenues of study. trait is essential for survival). Likewise, we need to continue to 1. Studies exploring how natural versus sexual selection affect study in depth how phenotypic variation exposed to selection primary defenses are not abundant, but are on the rise. In by receivers is induced and maintained. To do that, we need contrast, with a few exceptions (e.g., studies on the dual role of to define the life-history costs of production and maintenance pyrrolizine alkaloids in bella moths Utetheisa ornatrix; Conner of different multimodal-signal components under various biotic et al., 1981), less effort has been made to test the possible multiple and abiotic conditions (Hegna et al., 2013; Brain, 2016; Lindstedt functions of chemical compounds in chemical communication et al., 2016). This will give us key information on how much of between conspecifics and in predator deterrence. One potential the signal variation is environmentally induced. chemical group with multiple functions could be pyrazines, 4. Before the role of any signal in either predator deterrence a group of compounds that are relatively common in insect or mate attraction can be established, it is essential to identify defensive fluids (Rothschild et al., 1984; Guilford et al., 1987; and confirm the selective agent. Failure to properly do so can Moore et al., 1990; Vencl et al., 2016; Rojas et al., 2017). It is lead to misinterpretation or overestimation of the studied trait possible that, for example, the intensity of the repulsive odor function. Chemical defenses, for example, may have very rich produced by pyrazines could also function as an honest signal profiles with hundreds of compounds but, if relevant predators of quality. In those terms, a male with higher concentration of do not respond to them, then that defense is not under selection

Frontiers in Ecology and Evolution | www.frontiersin.org 16 July 2018 | Volume 6 | Article 93 Rojas et al. Aposematic Signals and Mate Attraction by predators. It is of curse possible that the relevant predator is combined with either warning colors or chemical defenses, may no longer present and we are thus witnessing the consequence have a key function in predator deterrence and interactions of past selection. Furthermore, we should keep in mind that between conspecifics in aposematic species. selective agents fluctuate across time and space (e.g., Endler and 7. Finally, the origin and spread of the first individuals bearing Rojas, 2009; Nokelainen et al., 2014). This means, for example, aposematic signals continues to be a matter of debate (Mappes that identifying a predator at a particular location does not imply et al., 2005; Speed and Ruxton, 2005). The first individuals with a it is a selective agent elsewhere. conspicuous warning coloration would have been an easy target 5. An integrative study of multimodal signal evolution should for predators, making it perplexing that they were able to multiply involve a better understanding of how signals are processed until they were numerous enough to prompt predator avoidance. by the receiver’s sensory systems. Recent advances in the field One potential solution for this problem is that natural and sexual of visual ecology (e.g., animal vision models; Vorobyev and selection could both favor the evolution of aposematic displays, Osorio, 1998; Kelber et al., 2003; Endler and Mielke, 2005; Maia and one way to tackle it is using phylogenetic comparative et al., 2013; Kemp et al., 2015; Troscianko and Stevens, 2015; methods. These methods have been used to study, for example, Renoult et al., 2017; Maia and White, 2018), as well as well- the correlated evolution of warning coloration and toxicity known and widely used methods in chemical ecology (Harborne, (Summers, 1987; Summers and Clough, 2001), but they would 1997; Agelopoulos and Pickett, 1998) offer the tools to study also be valuable to better understand how natural selection and if and how signals are discriminated against the background sexual selection have jointly shaped the evolution of multimodal noise. However, knowing that a signal can be perceived is warning displays. not enough. In addition to that, classic predation and mate choice experiments, particularly those in which the multiple AUTHOR CONTRIBUTIONS components of the warning display can be tested in isolation and in different combinations, can provide information about the BR, JM, CL, SG, EB-S, KR, and ON conceived the scope of the receiver’s response. Whether or not receivers react to the signals review. BR, CD, and LH collected information from the literature. sent by the emitter is what actually determines how these signals BR did the analyses and figures, and led the writing. All authors are shaped. contributed to the discussion of ideas, writing and editing the 6. The role of behavior in aposematic displays has been manuscript, and approved the final version of it. largely understudied, although it has the potential to be, if not a signal, a relevant cue for predators in combination ACKNOWLEDGMENTS with other components. Evidence from studies on mimicry has highlighted how mimics fool predators by mimicking the We are most grateful to Astrid Groot and Varvara Vedenina motion type of their models. Such is the case of ant-mimicking for the invitation to contribute to this special issue, to two spiders (genus Myrmarachne) of the family Salticidae, which reviewers, for their constructive and encouraging feedback, and are thought to mimic not only the morphology but also the to Oskar Brattström, Susan Finkbeiner, Eduard Florin Niga, characteristic movement of their ant models (Nelson and Card, JP Lawrence, Paul Marek, Pablo Palacios, Andrius Pašukonis, 2016); or of certain species of hover flies (family Syrphidae), Nicholas Scobel, and Ryan Taylor for kindly allowing us to use which mimic the behavior of wasps (Penney et al., 2014). While their photographs. Many thanks to Kaisa Suisto, Jimi Kirvesoja, both the Myrmarachne spiders and the hover flies are Batesian and all the greenhouse workers at the University of Jyväskylä (undefended) mimics, and thus not aposematic, they raise the who have made it possible to keep a healthy moth stock; and question of whether aposematic species do also use behavior as to Helinä Nisu for her invaluable help with the birds used a component of their warning displays. To date, we are aware in some of the experiments mentioned here. We gratefully of only one study in that direction: Neotropical aposematic acknowledge funding from the Centre of Excellence in Biological butterflies can be told apart by bird predators from their non- interactions (Academy of Finland, project no. 284666 to JM). BR aposematic counterparts on the basis of their flight behavior is particularly thankful to J. Stynoski and S. Calhim for ideas on (Chai, 1986), and it cannot be discarded that it also plays a role data visualization. We also thank the Academy of Finland for the in interactions between conspecifics, for example in courtship Post-Doctoral Fellow funding to ON (project no. 21000038821) displays. Therefore, behavior in general, and motion in particular, and SG (project no. 21000027441).

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Yang, Y., Richards-Zawacki, C. L., Devar, A., and Dugas, M. B. (2016). Zylinski, S., and Osorio, D. (2013). Visual contrast and color in rapid learning of Poison frog color morphs express assortative mate preferences in novel patterns by chicks. J. Exp. Biol. 216, 4184. doi: 10.1242/jeb.085001 allopatry but not sympatry. Evolution 70, 2778–2788. doi: 10.1111/evo. 13079 Conflict of Interest Statement: The authors declare that the research was Yoshimura, Y., and Kasuya, E. (2013). Odorous and non-fatal skin conducted in the absence of any commercial or financial relationships that could secretion of adult wrinkled frog (Rana rugosa) is effective in avoiding be construed as a potential conflict of interest. predation by snakes. PLoS ONE 8:e81280. doi: 10.1371/journal.pone.00 81280 Copyright © 2018 Rojas, Burdfield-Steel, De Pasqual, Gordon, Hernández, Mappes, Zagrobelny, M., Bak, S., Rasmussen, A. V., Jørgensen, B., Naumann, Nokelainen, Rönkä and Lindstedt. This is an open-access article distributed under the C. M., and Lindberg Møller, B. (2004). Cyanogenic glucosides terms of the Creative Commons Attribution License (CC BY). The use, distribution and plant–insect interactions. Phytochemistry 65, 293–306. or reproduction in other forums is permitted, provided the original author(s) and doi: 10.1016/j.phytochem.2003.10.016 the copyright owner(s) are credited and that the original publication in this journal Zuk, M., and Kolluru, G. R. (1998). Exploitation of sexual signals by predators and is cited, in accordance with accepted academic practice. No use, distribution or parasitoids. Q. Rev. Biol. 73, 415–438. doi: 10.1086/420412 reproduction is permitted which does not comply with these terms.

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